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Abstract

Background

Neurologists often diagnose brain death (BD) and explain BD to families in the intensive
care unit. This study was designed to determine whether neurologists agree with the
standard concept of death (irreversible loss of integrative unity of the organism)
and understand the state of the brain when BD is diagnosed.

Methods

A previously validated survey was mailed to a random sample of 500 board-certified
neurologists in the United States. Main outcomes were: responses indicating the concept
of death that BD fulfills and the empirical state of the brain that would rule out
BD.

Results

After the second mailing, 218 (44%) surveys were returned. Few (n = 52, 27%; 95% confidence
interval (CI), 21%, 34%) responded that BD is death because the organism has lost
integrative unity. The most common justification was a higher brain concept (n = 93,
48%; 95% CI, 41%, 55%), suggesting that irreversible loss of consciousness is death.
Contrary to the recent President's Council on Bioethics, few (n = 22, 12%; 95% CI,
8%, 17%) responded that the irreversible lack of vital work of an organism is a concept
of death that the BD criterion may satisfy. Many responded that certain brain functions
remaining are not compatible with a diagnosis of BD, including EEG activity, evoked
potential activity, and hypothalamic neuroendocrine function. Many also responded
that brain blood flow and lack of brainstem destruction are not compatible with a
diagnosis of BD.

Conclusions

American neurologists do not have a consistent rationale for accepting BD as death,
nor a clear understanding of diagnostic tests for BD.

Background

There are two ways to diagnose death: irreversible loss of circulation, and irreversible
loss of all functions of the brain, including the brainstem [1]. Each is a criterion for death, because it marks the univocal state of death, the
irreversible loss of the function of the organism as a whole. Integrative unity of
the organism, including resistance of entropy and maintenance of internal homeostasis,
is lost, leaving a mere collection of tissues and organs [1-4]. For medicine, law, and ethics, this is the written standard rationale for accepting
brain death (BD) as a criterion for death [1-4]. The tests used at the bedside to diagnose BD verify the irreversible loss of all
functions of the brain. Neurologists in the intensive care unit confirm BD by using
a clinical neurologic examination, and once diagnosed the patient is dead; this diagnosis
is "final and cannot be reversed. The person will never awaken [5]." Some authors have challenged this paradigm [3,4,6]. In response, neurologist groups have made it clear that BD conforms with the law
as written in the Uniform Determination of Death Act (UDDA), with "accepted medical
standards" [7-11] and that "it will be hard to find a physician closely involved with BD determination
and organ donation who does not think those [BD patients] are dead [9]."

We designed a survey to determine whether board-certified neurologists in the United
States agree with the standard concept of death (defined by the President's Commission
and neurologist groups as the irreversible loss of integrative unity of the organism
[1-4,6,10,11]), and understand the criterion of death (irreversible loss of all functions of the
brain, including the brainstem), and the empirical state of the brain diagnosed by
the tests used to confirm BD. We hypothesized that neurologists would not be aware
of the standard paradigm justifying the diagnosis of death and would not understand
the empirical state of patients determined dead based on the criterion of BD. This
is important because the American Academy of Neurology suggests that neurologists
have special expertise in declarations of BD [7,8].

Methods

Questionnaire administration

This study was a prospective survey of a random sampling of board-certified neurologists
in the United States regarding their opinions about BD. The mailing list was obtained
from Healthcare Lists Division SDI (Yardley, PA) in August 2009. Each neurologist
was mailed the survey in January 2010, along with a $5 gift certificate to encourage
them to have a coffee while filling out the questionnaire. A cover letter asked participants
to complete the survey and mail it back in the addressed, stamped envelope. A second
mailing was done in May 2010 to nonresponders. All responses were received by July
2010. The cover letter stated, "We are sending you a short questionnaire asking your
opinions around some of the concepts surrounding BD. We want to sample the opinions
regarding the concept of BD. Your responses are voluntary and confidential." The study
was approved by our university health ethics research board.

Questionnaire development

The development and initial testing of the instrument are described in more detail
elsewhere [12,13]. The current instrument (Additional File 1) is identical to that used in a survey of Canadian pediatric intensivists and Canadian
neurosurgeons, with the following changes: (a) in the first question about acceptable
conceptual reasons to explain BD, we added the choice "cessation of the vital work
of a living organism--the work of self preservation, achieved through the organism's
need driven commerce with the surrounding world" as stated by the President's Council;
and (b) we modified the scenario regarding family refusal to stop "life support" in
a brain-dead patient to describe continued support for 8 months until ventilator withdrawal,
and asked "was this patient dead for the last 8 months?" and if the patient, during
the last 8 months, was doing any of the three vital activities stated by the President's
Council to indicate life (Additional File 1) [14].

Additional file 1.Brain Death Survey. The survey sent out to American neurologists asking for their opinions regarding
brain death.

To generate the items for inclusion in the questionnaire, we searched MEDLINE from
1996 to 2004 for articles on BD, followed by review of the relevant article reference
lists. The new questions described above were based on the President's Council White
Paper [14]. To ensure clarity, realism, validity, and ease of completion, initial pilot testing
was done by having five local pediatric intensivists, one local pediatrician, and
one local organ donation coordinator complete the questionnaire, followed by a semistructured
interview for feedback.

Statistical analysis

Certain definitions were made a priori for two of the survey questions. The first
question asked the respondent to choose from a list of "stand-alone" reason(s) that
"is/are an acceptable conceptual reason to explain why 'brain death' is equivalent
to 'death'." The seventh question asked, "This patient fulfills all brain death criteria
unequivocally, including the suitable interval. Conceptually, why are they dead (i.e.,
in your own words, what is it about loss of brain function, including the brainstem,
that makes this patient dead)?" For analysis, we classified responses into categories
that have been discussed in the literature, including loss of integration concept
of BD, higher brain concept of BD, prognosis concept of BD, and statement of the criterion
only.

Results

The questionnaire was mailed to a random sample of 500 board-certified neurologists
in the United States; after the second mailing, 218 (44%) had been returned. Of the
218 returned, 26 (12%) did not have data that could be analyzed: 24 were returned
to sender, and 2 were returned blank. Therefore, there were 192 of 477 (40.3%) eligible
surveys returned with data for analysis.

The first question asked, "Which of several choices is an acceptable stand-alone conceptual
reason to explain why BD is equivalent to death." Fifty-two (27%; 95% CI, 21-34%)
chose the irreversible loss of the integration of body functions by the brain, 22
(12%; 8-17%) a cessation of the vital work of the organism, and almost half (48%;
41-55%) used a higher brain concept (Table 1).

Table 1. Responses to the question on conceptual reasons to explain why brain death is equivalent
to death

The next two questions asked about which objective test results, or pathology results
(in a patient maintained as BD for 48 hours), would not be compatible with BD. A majority
of respondents were unaware of the findings their patients may have when diagnosed
with BD (Table 2).

Table 2. The objective findings that respondents considered would not be compatible with brain
death

The next three questions asked about the timing of BD in different patient situations.
When faced with a patient who has EEG activity yet fulfills BD criteria, 26 (14%;
9-19%) consider the patient dead at the first BD examination, 72 (38%; 31-45%) at
the second examination, and 90 (47%; 40-54%) only when the EEG became isoelectric
12 hours later. When faced with a pregnant patient with BD supported for 11 weeks
until delivery, most agreed the patient was dead by the first (36, 19%; 14-25%) or
second (119, 62%; 55-69%) examination. However, in this brain-dead pregnant patient,
36 (19%; 14-25%) answered that she was not actually dead until sometime later: 11
(6%; 3-10%) after delivery of the neonate, 19 (10%; 6-15%) after organs are recovered
and the ventilator is stopped, and 6 (3%; 1-7%) at none of these times. When faced
with a brain-dead patient who has no cerebral blood flow but a family who insists
on continued life support for the next months, and asked "was this patient dead for
the last 8 months," 31 (16%; 12-22%) responded "no." When asked if this patient was
performing vital work during those months, 164 (85%; 80-90%) responded no, and 30
(15%; 11-21%) responded yes [receptive to stimuli, 9 (5%; 2-9%); acting upon the world,
5 (3%; 1-6%), and carrying out basic (non-conscious) felt needs, 16 (8%; 5-13%)].

The next two questions asked again about the underlying conceptual basis of BD: "In
your own words, what is it about loss of brain function including the brainstem that
makes this patient dead?" and "Prior to this survey, had you thought about why, at
a conceptual level, brain death is equivalent to death of the patient?" Only 21 (11%;
7-16%) of respondents had not previously thought about why BD is equivalent to death.
In their own words, only 15 (8%; 5-13%) used a loss of integration concept (Table
3).

Table 3. Response to the question about what, in the respondent's own words, makes a patient
dead

The next question asked which choice "best describes why you are comfortable diagnosing
death based on the criteria of brain death?" Most (133, 69%; 62-75%) responded that
"the conceptual basis of brain death makes it equivalent to death of the patient."
Many responded that the reason is because it is a standard: an accepted medical standard
(46, 24%; 18-30%), an accepted legal standard (24, 13%; 8-18%), and/or "the diagnosis
of brain death was taught to me during my training" (14, 7%; 4-12%). Five (3%; 1-6%)
were not comfortable diagnosing death based on BD.

The final question asked: "Are brain death and cardiac death the same state (i.e.,
are both death of the patient)?" More than half (104, 54%; 47-61%) chose "no," 86
(45%; 38-52%) chose "yes," and 2 (1%; 0-4%) left the answer blank.

Further analysis was done for those 133 (69%) who responded that they were comfortable
diagnosing BD, because "the conceptual basis of brain death makes it equivalent to
death of the patient." Their responses to the question asking to state the concept
of BD in their own words is shown in Table 3. Only 13 (10%; 6-16%) used a loss of integration concept, and 59 (44%; 36-53%) did
not articulate a concept (i.e., used a restatement of the criterion or left no response).
On the first question, only 39 (29%; 22-38%) considered "irreversible loss of the
integration of body functions by the brain" as an acceptable conceptual reason to
explain BD being equivalent to death and 67 (50%; 42-59%) chose a higher brain conceptual
reason.

Discussion

The American Academy of Neurology recently updated their evidence-based guideline
for determining BD in adults, reaffirming that irreversible cessation of all functions
of the entire brain, including the brainstem, can be determined "based on straightforward
principles," and is death [8]. This survey suggests that there are several potential flaws with this claim. First,
most neurologists do not understand (at best) or disagree (at worst) with the standard
concept that BD is death because the organism has lost integrative unity. The most
common justification given by neurologists was a higher brain concept, suggesting
that irreversible loss of consciousness is death. Very few neurologists consider the
irreversible lack of vital work of an organism as a concept of death that the BD criterion
may satisfy. Second, most neurologists do not understand (at best) or disagree (at
worst) that certain brain functions, including EEG activity, evoked potential activity,
and hypothalamic neuroendocrine function, often can remain in patients diagnosed dead
using accepted tests that have confirmed the BD criterion [15]. This suggests that these neurologists think that clinical tests for BD produce many
false-positive diagnoses of death. Third, most neurologists did not understand (at
best) or disagree (at worst) that brain blood flow and lack of brain destruction often
can occur in patients diagnosed dead using accepted tests confirming the BD criterion
[15,16]. This suggests that there may be concern (or confusion) about whether BD marks the
point of irreversible loss of brain functions. Finally, most neurologists do not consider
the criterion BD and circulatory death as each diagnostic of the univocal state of
death.

The concept of death

BD is said to be death by most professional bodies because it satisfies the concept/definition
of death (Table 4): loss of integrative unity of the organism as a whole, marking when an organism
is no longer an organism because it no longer can resist the forces of entropy and
no longer can maintain internal homeostasis [1-4]. Many have argued that integrative unity of the organism as a whole often continues
during BD (hence, integration is not dependent on functions of the brain), and a central
integrator is not required for life; therefore, many no longer consider this a concept
of death that BD satisfies [3,6,14]. Loss of personhood, based on irreversible loss of consciousness (sentience, or agency)
is necessary, but not sufficient, for death (Table 4) [3,4]. Although nonconscious patients may be allowed to die due to their profound neurological
disability, no society has accepted that they are already dead. It may be true that
BD patients have poor quality of life or certainty of cardiac arrest in a short period;
however, this denotes a prognosis and not a diagnosis of death. The President's Council
suggested a novel concept of death: that vital external work of an organism is required
to be alive, and once an organism no longer interacts with the environment to obtain
what it needs to survive, it is dead [14]. Importantly, simply restating the criterion of BD does not give any concept of death
that BD satisfies to justify BD being death.

Table 4. Conceptual and empirical arguments in favor of brain death, and problems with those
arguments

This survey shows that neurologists do not understand if, or disagree whether, the
criterion BD fulfils a concept of death. Few consider irreversible loss of integration
of the organism as a whole or irreversible loss of the ability to perform external
vital work as a reason to accept BD as death (some even consider that external work
continues during BD). Many confused a restatement of the criterion of BD as justification
that it is death, and a few conflated the prognosis of death with the diagnosis of
death. Most consider a higher brain concept of death justified. This is concerning
because neurologists often are the specialist declaring BD and explaining it to families
in the intensive care unit.

The tests of BD

The tests for BD are performed to confirm that irreversible loss of all functions
of the brain, including the brainstem, has occurred. It has been shown that some brain
functions continue after accurately clinically diagnosed BD, including EEG activity
in 20%, evoked potential activity in 5%, and hypothalamic neuroendocrine function
in > 50% [15]. These activities may be explained by the finding that continued brain blood flow
occurs in 5-40% of BD patients, and pathologic destruction of brain does not occur
in more than 40% of BD patients (even after over 24-48 hr of maintained circulation)
[15,16]. The ongoing brain functions have been explained with several controversial claims
(Table 4) [3,4,15,17-19]. First, these are mere activities and not functions; however, the brain seems too complex an organ to simply make this
claim [3,17]. Second, these are insignificant functions; however, this is an ad hoc claim [3,4,15,17]. Third, these are not critical clinical functions, and BD is a clinical diagnosis; however, this claim is both ad hoc and
circular (critical clinical functions are necessary for maintenance of life, and death
is the loss of critical clinical functions, is a trivial tautologous statement) [3,17]. Fourth, these are not critical functions, because they are replaceable mechanically; however, this would only lead to a higher brain consciousness based
concept of death [3,4,15,17-19].

This survey shows that most neurologists do not understand, or disagree, that certain
brain functions can remain in patients diagnosed dead using accepted clinical tests
confirming the BD criterion. This may suggest that the accepted medical standard of
clinical tests for BD can produce false-positive diagnoses of death. At the very least,
the neurologists often are unaware of (or worse, disagree with) the debates regarding
the meaning of significant, critical, clinical, brain functions.

Other potential interpretations

First, we assumed that there is a "standard concept of death." However, we included
in the survey all the concepts offered in the literature and also provided an opportunity
to provide a new concept in the open-ended question. Although we found that most neurologists
did not agree with the concept of loss of integrative unity, the main alternative
was a higher brain concept. This would imply that patients with permanent vegetative
state are dead in their state of wakefulness and breathing. Second, perhaps the finding
that 97% of neurologists are comfortable diagnosing death based on BD only shows that
neurologists are not able to justify explicitly why the equivalency truly holds. After
all, this is a philosophical question and may not involve terminology used in clinical
training. Perhaps the main finding of the survey is uncovering an unmet neurologists'
educational need. Although a potential interpretation, this may not be reassuring
to families who are told that their loved one is dead based on the criterion BD. In
addition, the American Board of Psychiatry and Neurology lists an understanding of
BD on the objectives of training [20]. Third, although the survey did not determine this, perhaps neurologists accept BD
as "dead enough" for organ donation and withdrawal of life-support purposes. Accordingly,
patients with BD should be allowed to die or should be treated as if they no longer
are part of the human moral community; but, this is different than being biologically
dead. We agree with other authors who have suggested that if BD is not death, whether
BD can be considered a state where vital organ donation complies with nonmaleficence
(death is an unavoidable and minimal harm) and autonomy (with informed consent) requires
further discussion and debate [21].

Limitations and strengths

The relatively small sample size, only modest response rate to this survey, and lack
of information regarding respondents' exposure to BD patients are significant limitations.
In addition, the closed-ended questions may not have allowed respondents to elaborate
and clarify their responses. The strengths of the survey include the development methodology,
and unambiguous nature of most of the questions. In addition, the striking similarity
of our results to those of other surveys done in the past, including using this same
survey in different populations of North American nonneurologist medical specialists,
enhances the generalizability of the results [12,13,22-24]. The preponderance of evidence from this survey, and other surveys, support the conclusions
we have drawn.

Conclusions

Neurologists do not have a consistent rationale for accepting BD as death, nor a clear
understanding of the diagnostic tests for BD. Almost half accept BD because it is
a state of permanent unconsciousness, and more than half do not consider it equivalent
to circulatory death. Wijdicks, in explaining that BD is a clinical diagnosis, and
that confirmatory tests are not needed, asks "So, what are neurologists confirming?"
[25]. Unfortunately, he does not answer this question, and only claims that "confirmatory
tests do not confirm anything [because BD] is synonymous with a certain clinical state
[from which] there are no recoveries on record.... [25]" Similarly, the American Academy of Neurology and the Canadian Forum Brain Death
Guidelines suggest that BD is death because of its prognosis (claiming it is irreversible)
and lack of consciousness [7,8,26]. If BD is death, a conceptual rationale for this should be clarified. This has important
ethical implications for the practice of intensive care medicine.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

ARJ designed the study, analyzed the data, and drafted the manuscript. All authors
(ARJ, NRA, JPD, ARD) contributed to study conception and design, acquisition of data,
interpretation of data, revised the manuscript critically for important intellectual
content, and have given final approval of the version to be published.

Acknowledgements

There was no source of funding for this project. AJ had full access to all the data
in the study and takes responsibility for the integrity of the data and the accuracy
of the data analysis. Preliminary results of this study were presented as a poster
at the American Thoracic Society conference, Denver, Colorado, USA, in May 2011.

References

President's Commission for the Study of Ethical Problems in Medicine and Biomedical
and Behavioral Research: Defining Death: Medical, Legal and Ethical Issues in the Determination of Death. Washington, DC: U.S. Government Printing Office; 1981.

Bernat JL, Culver CM, Gert B: On the definition and criterion of death.